The Unique Antimicrobial Recognition and Signaling Pathways in Tardigrades with a Comparison Across Ecdysozoa

Abstract

Tardigrades are microscopic animals known to withstand unfavorable abiotic conditions. These animals are also constantly exposed to biotic stresses, including parasites and internal microbiomes. However, the tardigrade immune mechanisms against these biotic stresses are largely uncharacterized. Due to the contentious phylogenetic position of tardigrades, it is not intuitive whether they possess an immune system more similar to that of arthropods (e.g., Toll, Imd, and JNK pathways of the Drosophila melanogaster antimicrobial response) or to that of nematodes (e.g., the Tir-1/Nsy-1/Sek-1/Pmk-1/Atf-7 signaling cassette [called Tir-1 pathway here]) in Caenorhabditis elegans). In this study, comparative genomic analyses were conducted to mine homologs of canonical D. melanogaster and C. elegans immune pathway genes from eight tardigrades (Echiniscoides cf. sigismundi, Echiniscus testudo, Hypsibius exemplaris, Mesobiotus philippinicus, Milnesium tardigradum, Paramacrobiotus richtersi, Richtersius cf. coronifer, and Ramazzottius varieornatus) and four non-arthropod ecdysozoans (two onychophorans: Epiperipatus sp. and Opisthopatus kwazululandi; one nematomorph: Paragordius varius; and one priapulan: Priapulus caudatus) in order to provide insights into the tardigrade antimicrobial system. No homologs of the intracellular components of the Toll pathway were detected in any of the tardigrades examined. Likewise, no homologs of most of the Imd pathway genes were detected in any of the tardigrades or any of the other non-arthropod ecdysozoans. Both the JNK and Tir-1 pathways, on the other hand, were found to be conserved across ecdysozoans. Interestingly, tardigrades had no detectable homologs of NF-κB, the major activator of antimicrobial response gene expression. Instead, tardigrades appear to possess NF-κB distantly related NFAT homologs. Overall, our results show that tardigrades have a unique gene pathway repertoire that differs from that of other ecdysozoans. Our study also provides a framework for future studies on tardigrade immune responses.

Phlebotomus papatasi Antimicrobial Peptides in Larvae and Females and a Gut-Specific Defensin Upregulated by Leishmania major Infection

“…They form a group closely related to mosquitoes in both cases while less similar to other flies such as Drosophila and Stomoxys. Phylogenetic analyses of these transcription factors commonly show mosquito sequences forming a separate branch from Drosophila species [42] and more distantly related to other insects such as Nasonia vitripennis and Tribolium castaneum species [43]. These findings suggest that these sand fly and mosquito transcription factors evolved from a common ancestor.…”

The genome of the brackish-water malaria vectorAnopheles aquasalis

“…In general, the family groups related to reactive oxygen species production control processes, and components regulating the expression of effectors of the immune response or signaling pathways were well conserved, with groupings of orthologs 1:1 for the four species. They are functionally relevant genes for the maintenance of the homeostasis of the organism, and in the case of signaling pathways such as the Toll pathway, they help in embryonic development processes, being constitutive for these insects (28)(29)(30). On the other hand, the marked differences in the number of copies were in groups related to the recognition of molecular patterns of microorganisms, with sharp differences in the FREP and MLD proteins, especially with species-specific expansions in An.…”

Tardigrades and Their Emergence as Model Organisms

“…And although tardigrades likely lost major body regions that were present in ancestors, the developmental and evolutionary mechanisms that led to such losses are incompletely understood. Tardigrades will likely continue to be useful along with other organisms to help trace evolutionary changes in the arthropods and nematodes, and more generally to aid in establishing the gene complement, development, and morphology of ancestors at various nodes of animal phylogeny (see for example Bavan et al, 2009;Hering and Mayer, 2014;Gross and Mayer, 2015;Thiruketheeswaran et al, 2016;Hering et al, 2016;Nelson, 2017;Smith et al, 2017;Koziol, 2018;Mapalo et al, 2020).…”